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OPEN
Cross shelf benthic biodiversity patterns in the Southern Red Sea Joanne Ellis1, Holger Anlauf1, Saskia Kürten1, Diego Lozano-Cortés2, Zahra Alsaffar1, Joao Cúrdia1, Burton Jones1 & Susana Carvalho1
Received: 5 October 2016 Accepted: 2 March 2017 Published: xx xx xxxx
The diversity of coral reef and soft sediment ecosystems in the Red Sea has to date received limited scientific attention. This study investigates changes in the community composition of both reef and macrobenthic communities along a cross shelf gradient. Coral reef assemblages differed significantly in species composition and structure with location and depth. Inner shelf reefs harbored less abundant and less diverse coral assemblages with higher percentage macroalgae cover. Nutrient availability and distance from the shoreline were significantly related to changes in coral composition and structure. This study also observed a clear inshore offshore pattern for soft sediment communities. In contrast to the coral reef patterns the highest diversity and abundance of soft sediment communities were recorded at the inshore sites, which were characterized by a higher number of opportunistic polychaete species and bivalves indicative of mild disturbance. Sediment grain size and nutrient enrichment were important variables explaining the variability. This study aims to contribute to our understanding of ecosystem processes and biodiversity in the Red Sea region in an area that also has the potential to provide insight into pressing topics, such as the capacity of reef systems and benthic macrofaunal organisms to adapt to global climate change. The Red Sea is a confined water body by the Arabian Peninsula and African mainland, stretching from 30°N to 12°40′N over 1900 km and reaching a maximum width of 335 km1. Its latitude extension and arid continental setting make the Red Sea experience high rates of evaporation, a wide range of seasonal shallow water temperature regimes from 18 to 32 °C and above global ocean average saline conditions in the range of 37 to 42 psu2, 3. There is limited coastal runoff of freshwater into the Red Sea therefore the water loss of 2 m year−1 by evaporation is replenished almost entirely by oceanic waters from the Mediterranean via the Suez Canal and from the Indian Ocean by the narrow Bab-al-Mandab Strait4, 5. These combined conditions make the Red Sea one of the world’s warmest and most saline habitats in which extensive coral reefs occur, and therefore also a region of increasing interest for scientists working on climate change. Much of the information on the Red Sea lies within technical reports, and there is relatively little information available to researchers using modern channels6. The Red Sea region is also relatively inaccessible due to permitting regulations and therefore remains a poorly studied system6. Further, the vast majority of published research for coral assemblages originates from an approximately 6 km stretch of the coastline in the far northern Red Sea near the Gulf of Aqaba while the literature on the soft sediment benthos of the Red Sea has been reported as very limited. Despite these research limitations, the Red Sea has long been recognized ecologically as one of the world’s biodiversity hotspots and an area of high endemism7–9. More than 364 scleractinian coral species (hard corals) have been recorded; of which 5.8% were suggested to be endemic9. Additionally, new reports of endemic scleractinian corals support that high levels of speciation exist in the Red Sea10. A few early studies have provided initial records on the abundance of soft sediment macrobenthos in the region and also provided support for high levels of soft sediment benthic species diversity11, 12. There is still a current lack of understanding of the general ecology of the Red Sea despite the region’s high biodiversity6. Increasingly anthropogenic impacts are affecting the ecology of the Red Sea region including rapid human population growth and urbanization, coastal construction, tourism, reef over-usage13 and destructive fisheries14. Thus, marine resource management priorities and the urgent need for monitoring programs have been identified as of high importance for the Red Sea region15. As part of a recent initiative between the Red Sea Research Centre and Saudi Aramco, regional assessments have been undertaken to characterise the Red Sea environment for marine spatial planning efforts and to provide 1
King Abdullah University of Science and Technology (KAUST), Red Sea Research Center, Division of Biological and Environmental Science and Engineering, Thuwal, 23955-6900, Saudi Arabia. 2Environmental Protection Department, Saudi Aramco, Dhahran, 31311, Saudi Arabia. Correspondence and requests for materials should be addressed to J.E. (email: [email protected]) Scientific Reports | 7: 437 | DOI:10.1038/s41598-017-00507-y
1
www.nature.com/scientificreports/
Figure 1. Map showing the location of the reef and soft sediment sites sampled across the Farasan shelf in the southern Red Sea. This figure was created using the ArcGIS software (ArcMap 10.3.1) by ESRI, Inc. (ESRI.com), GEBCO, DeLorme, US Geological Survey (USGS) and the National Oceanic and Atmospheric Administration (NOAA) photo library.
baseline information for future monitoring programs. In this study, we assessed regional biodiversity patterns from both coral reef and soft sediment data collected across a shelf gradient in the Farasan Islands. Spatial patterns in the distribution and abundance of species have been reported to change significantly over cross shelf gradients16, however the underlying drivers of species change across these gradients has not previously been fully assessed. There has been an increasing focus worldwide on regional assessments of biodiversity that can link the role of environmental variables in structuring community composition17. The understanding of regional biodiversity patterns and species distribution relative to their habitat is fundamental18 providing data that could inform science-based management approaches6. Most diversity studies across coastal shelves have, however, focused on single taxonomic groups, such as corals, with very few studies assessing multi-taxon diversity patterns in a marine context (exceptions include19, 20). Multi-taxon studies addressing the dynamic structuring of ecological communities have been beneficially utilized in testing and implementing high-quality conservation strategies19. Within this study, we present results of coral reef surveys following a longitudinal gradient at the Farasan Islands, ranging from inshore to offshore locations. We also present cross shelf biodiversity data collected from soft sediment macrobenthic assemblages investigating environmental variables that influence species distribution. The specific aims of this paper are to: (a) provide baseline information on both coral reef and soft sediment biodiversity patterns for the Red Sea region where there is limited information published; (b) to assess soft sediment and coral reef diversity patterns across a shelf gradient; and (c) to identify the role of environmental variables in structuring coral reef and soft sediment benthic communities. The present study aims to contribute to a better understanding of ecosystem processes and current biodiversity in the southern Red Sea region, an area that has the potential to provide insight into pressing topics such as the capacity of reef systems and benthic macrofaunal organisms to adapt to global climate change. This is, to our knowledge, the first synoptic study of benthic soft sediment faunal species richness and benthic coral reef diversity in the Red Sea that also relates biodiversity patterns to environmental and hydrographic variables.
Material and Methods
Study area. Soft sediment and reef surveys were conducted in the southern Red Sea to assess cross shelf gradient biodiversity patterns. The study area included sites around the Jazan City region and the Farasan Island Marine Sanctuary (Fig. 1). The wider Jazan province has a population of approximately 1.5 million and covers an area of 40,000 km2. Jazan City is an urbanized area with agricultural activities also present in the region. Three of the main islands at the Farasan Island Marine Sanctuary are permanently inhabited (Farasan, 369 km2; Sajid, 109 km2; Qummah, 14.3 km2) with a total population of approximately 4,500 inhabitants. Despite being considered a Marine Sanctuary, most of the inhabitants engage in fishing and agricultural activities. The Farasan Island plateau slopes gently over a distance of 120 km never reaching water depths greater than 200 m21. Reef survey. Quantitative surveys of benthic reef community. Coral reefs were assessed in February and
September 2014. A total of 11 reef locations, six in the inner shelf (IS; IS1, IS2, IS3, IS4, IS5, IS6) and five in the outer shelf (OS; OS1, OS2, OS3, OS4, OS5), were surveyed using a 1 m wide photo quadrate belt-transect (Fig. 1). The transect line ideally followed the depth horizons at 3–5 m and 8–10 m. At some locations only the shallow transect was completed because a limestone reef foundation did not exist at deeper locations. Three replicate 20 m by 5 m transects comprised the surveyed 60 m2 along a horizontal stretch of slope at each reef site and depth. Along each transect, a photo (1 m2) was taken every two meters with a Canon G16 16 megapixel digital camera in Nauticam housing. The benthic community was assessed based on 90 benthic groups including scleractinian coral genera, abundant soft coral genera and other benthic community groups. Quantification and identification Scientific Reports | 7: 437 | DOI:10.1038/s41598-017-00507-y
2
www.nature.com/scientificreports/ Benthic Component Abiotic
Category Rock Sand Algal assemblage Coralline algae
Algae
Halimeda Macroalgae Sargassum Turf algae
Coral
Soft coral Scleractinian Dead coral
Dead coral
Dead coral with algae Rubble Anemones Ascidians Bivalve
Invertebrates
Hydroids Sponge Zoanthids Other invertebrates
Seagrass
Seagrass
Table 1. Main categories used to define benthic community composition. of benthic groups along each transect replicate utilized the software Coral Point Count with Excel extensions (CPCe22), with 40 randomly distributed points per 1 m2 frame. Coral identification was undertaken at family level for Fungidae or genus level for other Scleractinia following Veron23 despite the current revisions on coral’s taxonomy being undertaken worldwide. Counted points were averaged for each site and depth to calculate percentage cover of each group including corals (calcifying corals including Millipora), soft corals, sponges, coralline algae, turf algae, macroalgae and the abiotic components sand, rock and rubble. Forty points were randomly distributed on each substrate image and the features underlying the points user-identified. Overall, per photo-transect, benthic community composition was analyzed in terms of number of Operational Taxonomic Units (OTUs), cover of corals (both soft and scleractinian), sponges, hydroids and other invertebrates (e.g. bivalves, echinoderms), algae (subdivided by the following functional groups: macroalgae, turf, coralline algae) (see Table 1 for main benthic categories). Water samples for nutrients and Chlorophyll a were also collected from surface waters at each reef site (see water sampling methods below). Size frequency distribution of corals. Negatively skewed size-frequency distributions in coral populations have been associated with unfavorable environmental conditions. Using the same photoquadrat data, we compared the size-frequency distributions between near shore and offshore reefs in the four most abundant genera (Acropora, Echinopora, Porites and Galaxea) to explore the occurrence of any differences in the skewness of the size distribution of the corals as a proxy for different environmental conditions. The colony diameter (maximum and minimum) was measured using the software ImageJ to estimate the colony area (projected surface area). Colony area was estimated using the half-sphere formula (Colony area = 2 × [(maximum diameter/2 × minimum diameter/2) × π]) following Lozano-Cortés & Berumen24. The projected surface area data was logarithmically transformed and from these data, size-frequency distributions were constructed25 and its skewness (g1) calculated26.
Soft sediment macrobenthic survey. Sediment samples from 13 stations (Fig. 1) were collected across an inshore to offshore transect from Jazan to the Farasan Islands using a 0.1 m2 Van Veen grab (two replicates at each site) and sieved through a 1 mm mesh screen. A total of 14 soft sediment stations were sampled. Sites located in the inner shelf include JAZ2, JAZ3, JAZ4, JAZ6, JAZ7, JAZ8, FI1, FI2, FI3, FI4, FI5 while sites located in the outer shelf included FI6, FI7, FI8. Samples were preserved in 96% ethanol. Sediment sub-samples from each replicate were taken for grain-size analysis, organic matter content (loss on ignition) and metals. Conductivity Temperature Depth (CTD) vertical casts were carried out at each station. The CTD casts recorded conductivity, temperature, depth and oxygen of the water column. Water samples were also taken for nutrients and chlorophyll a from the surface and the bottom layers (see below). In the laboratory, each sample was hand-sorted and then organisms identified using a stereomicroscope. Macrofauna were generally identified to the species level where possible or family level (see Supplementary Material). Sediment grain size was determined by wet sieving and calculation of dry weight percentage fractions following the Wentworth scale27. Grain size fractions were gravel (>2 mm), very coarse sand (1 mm), coarse sand (500 μm), medium sand (250 μm), fine sand (125 μm), very fine sand (63 μm) and silt-clay (8–10 m inner shelf (Table 3). Changes in size frequency and skewness. The corals surveyed ranged in diameter from 3 to 175 cm (Table 4). Statistically significant differences were detected between the size of the colonies from nearshore and offshore reefs for Acropora, Echinopora and Porites (Table 4). Smaller colonies were recorded in the nearshore reefs (Table 4). Juvenile coral density (mean ± SD) differed significantly between types of reefs for Acropora and Echinopora (p
OPEN
Cross shelf benthic biodiversity patterns in the Southern Red Sea Joanne Ellis1, Holger Anlauf1, Saskia Kürten1, Diego Lozano-Cortés2, Zahra Alsaffar1, Joao Cúrdia1, Burton Jones1 & Susana Carvalho1
Received: 5 October 2016 Accepted: 2 March 2017 Published: xx xx xxxx
The diversity of coral reef and soft sediment ecosystems in the Red Sea has to date received limited scientific attention. This study investigates changes in the community composition of both reef and macrobenthic communities along a cross shelf gradient. Coral reef assemblages differed significantly in species composition and structure with location and depth. Inner shelf reefs harbored less abundant and less diverse coral assemblages with higher percentage macroalgae cover. Nutrient availability and distance from the shoreline were significantly related to changes in coral composition and structure. This study also observed a clear inshore offshore pattern for soft sediment communities. In contrast to the coral reef patterns the highest diversity and abundance of soft sediment communities were recorded at the inshore sites, which were characterized by a higher number of opportunistic polychaete species and bivalves indicative of mild disturbance. Sediment grain size and nutrient enrichment were important variables explaining the variability. This study aims to contribute to our understanding of ecosystem processes and biodiversity in the Red Sea region in an area that also has the potential to provide insight into pressing topics, such as the capacity of reef systems and benthic macrofaunal organisms to adapt to global climate change. The Red Sea is a confined water body by the Arabian Peninsula and African mainland, stretching from 30°N to 12°40′N over 1900 km and reaching a maximum width of 335 km1. Its latitude extension and arid continental setting make the Red Sea experience high rates of evaporation, a wide range of seasonal shallow water temperature regimes from 18 to 32 °C and above global ocean average saline conditions in the range of 37 to 42 psu2, 3. There is limited coastal runoff of freshwater into the Red Sea therefore the water loss of 2 m year−1 by evaporation is replenished almost entirely by oceanic waters from the Mediterranean via the Suez Canal and from the Indian Ocean by the narrow Bab-al-Mandab Strait4, 5. These combined conditions make the Red Sea one of the world’s warmest and most saline habitats in which extensive coral reefs occur, and therefore also a region of increasing interest for scientists working on climate change. Much of the information on the Red Sea lies within technical reports, and there is relatively little information available to researchers using modern channels6. The Red Sea region is also relatively inaccessible due to permitting regulations and therefore remains a poorly studied system6. Further, the vast majority of published research for coral assemblages originates from an approximately 6 km stretch of the coastline in the far northern Red Sea near the Gulf of Aqaba while the literature on the soft sediment benthos of the Red Sea has been reported as very limited. Despite these research limitations, the Red Sea has long been recognized ecologically as one of the world’s biodiversity hotspots and an area of high endemism7–9. More than 364 scleractinian coral species (hard corals) have been recorded; of which 5.8% were suggested to be endemic9. Additionally, new reports of endemic scleractinian corals support that high levels of speciation exist in the Red Sea10. A few early studies have provided initial records on the abundance of soft sediment macrobenthos in the region and also provided support for high levels of soft sediment benthic species diversity11, 12. There is still a current lack of understanding of the general ecology of the Red Sea despite the region’s high biodiversity6. Increasingly anthropogenic impacts are affecting the ecology of the Red Sea region including rapid human population growth and urbanization, coastal construction, tourism, reef over-usage13 and destructive fisheries14. Thus, marine resource management priorities and the urgent need for monitoring programs have been identified as of high importance for the Red Sea region15. As part of a recent initiative between the Red Sea Research Centre and Saudi Aramco, regional assessments have been undertaken to characterise the Red Sea environment for marine spatial planning efforts and to provide 1
King Abdullah University of Science and Technology (KAUST), Red Sea Research Center, Division of Biological and Environmental Science and Engineering, Thuwal, 23955-6900, Saudi Arabia. 2Environmental Protection Department, Saudi Aramco, Dhahran, 31311, Saudi Arabia. Correspondence and requests for materials should be addressed to J.E. (email: [email protected]) Scientific Reports | 7: 437 | DOI:10.1038/s41598-017-00507-y
1
www.nature.com/scientificreports/
Figure 1. Map showing the location of the reef and soft sediment sites sampled across the Farasan shelf in the southern Red Sea. This figure was created using the ArcGIS software (ArcMap 10.3.1) by ESRI, Inc. (ESRI.com), GEBCO, DeLorme, US Geological Survey (USGS) and the National Oceanic and Atmospheric Administration (NOAA) photo library.
baseline information for future monitoring programs. In this study, we assessed regional biodiversity patterns from both coral reef and soft sediment data collected across a shelf gradient in the Farasan Islands. Spatial patterns in the distribution and abundance of species have been reported to change significantly over cross shelf gradients16, however the underlying drivers of species change across these gradients has not previously been fully assessed. There has been an increasing focus worldwide on regional assessments of biodiversity that can link the role of environmental variables in structuring community composition17. The understanding of regional biodiversity patterns and species distribution relative to their habitat is fundamental18 providing data that could inform science-based management approaches6. Most diversity studies across coastal shelves have, however, focused on single taxonomic groups, such as corals, with very few studies assessing multi-taxon diversity patterns in a marine context (exceptions include19, 20). Multi-taxon studies addressing the dynamic structuring of ecological communities have been beneficially utilized in testing and implementing high-quality conservation strategies19. Within this study, we present results of coral reef surveys following a longitudinal gradient at the Farasan Islands, ranging from inshore to offshore locations. We also present cross shelf biodiversity data collected from soft sediment macrobenthic assemblages investigating environmental variables that influence species distribution. The specific aims of this paper are to: (a) provide baseline information on both coral reef and soft sediment biodiversity patterns for the Red Sea region where there is limited information published; (b) to assess soft sediment and coral reef diversity patterns across a shelf gradient; and (c) to identify the role of environmental variables in structuring coral reef and soft sediment benthic communities. The present study aims to contribute to a better understanding of ecosystem processes and current biodiversity in the southern Red Sea region, an area that has the potential to provide insight into pressing topics such as the capacity of reef systems and benthic macrofaunal organisms to adapt to global climate change. This is, to our knowledge, the first synoptic study of benthic soft sediment faunal species richness and benthic coral reef diversity in the Red Sea that also relates biodiversity patterns to environmental and hydrographic variables.
Material and Methods
Study area. Soft sediment and reef surveys were conducted in the southern Red Sea to assess cross shelf gradient biodiversity patterns. The study area included sites around the Jazan City region and the Farasan Island Marine Sanctuary (Fig. 1). The wider Jazan province has a population of approximately 1.5 million and covers an area of 40,000 km2. Jazan City is an urbanized area with agricultural activities also present in the region. Three of the main islands at the Farasan Island Marine Sanctuary are permanently inhabited (Farasan, 369 km2; Sajid, 109 km2; Qummah, 14.3 km2) with a total population of approximately 4,500 inhabitants. Despite being considered a Marine Sanctuary, most of the inhabitants engage in fishing and agricultural activities. The Farasan Island plateau slopes gently over a distance of 120 km never reaching water depths greater than 200 m21. Reef survey. Quantitative surveys of benthic reef community. Coral reefs were assessed in February and
September 2014. A total of 11 reef locations, six in the inner shelf (IS; IS1, IS2, IS3, IS4, IS5, IS6) and five in the outer shelf (OS; OS1, OS2, OS3, OS4, OS5), were surveyed using a 1 m wide photo quadrate belt-transect (Fig. 1). The transect line ideally followed the depth horizons at 3–5 m and 8–10 m. At some locations only the shallow transect was completed because a limestone reef foundation did not exist at deeper locations. Three replicate 20 m by 5 m transects comprised the surveyed 60 m2 along a horizontal stretch of slope at each reef site and depth. Along each transect, a photo (1 m2) was taken every two meters with a Canon G16 16 megapixel digital camera in Nauticam housing. The benthic community was assessed based on 90 benthic groups including scleractinian coral genera, abundant soft coral genera and other benthic community groups. Quantification and identification Scientific Reports | 7: 437 | DOI:10.1038/s41598-017-00507-y
2
www.nature.com/scientificreports/ Benthic Component Abiotic
Category Rock Sand Algal assemblage Coralline algae
Algae
Halimeda Macroalgae Sargassum Turf algae
Coral
Soft coral Scleractinian Dead coral
Dead coral
Dead coral with algae Rubble Anemones Ascidians Bivalve
Invertebrates
Hydroids Sponge Zoanthids Other invertebrates
Seagrass
Seagrass
Table 1. Main categories used to define benthic community composition. of benthic groups along each transect replicate utilized the software Coral Point Count with Excel extensions (CPCe22), with 40 randomly distributed points per 1 m2 frame. Coral identification was undertaken at family level for Fungidae or genus level for other Scleractinia following Veron23 despite the current revisions on coral’s taxonomy being undertaken worldwide. Counted points were averaged for each site and depth to calculate percentage cover of each group including corals (calcifying corals including Millipora), soft corals, sponges, coralline algae, turf algae, macroalgae and the abiotic components sand, rock and rubble. Forty points were randomly distributed on each substrate image and the features underlying the points user-identified. Overall, per photo-transect, benthic community composition was analyzed in terms of number of Operational Taxonomic Units (OTUs), cover of corals (both soft and scleractinian), sponges, hydroids and other invertebrates (e.g. bivalves, echinoderms), algae (subdivided by the following functional groups: macroalgae, turf, coralline algae) (see Table 1 for main benthic categories). Water samples for nutrients and Chlorophyll a were also collected from surface waters at each reef site (see water sampling methods below). Size frequency distribution of corals. Negatively skewed size-frequency distributions in coral populations have been associated with unfavorable environmental conditions. Using the same photoquadrat data, we compared the size-frequency distributions between near shore and offshore reefs in the four most abundant genera (Acropora, Echinopora, Porites and Galaxea) to explore the occurrence of any differences in the skewness of the size distribution of the corals as a proxy for different environmental conditions. The colony diameter (maximum and minimum) was measured using the software ImageJ to estimate the colony area (projected surface area). Colony area was estimated using the half-sphere formula (Colony area = 2 × [(maximum diameter/2 × minimum diameter/2) × π]) following Lozano-Cortés & Berumen24. The projected surface area data was logarithmically transformed and from these data, size-frequency distributions were constructed25 and its skewness (g1) calculated26.
Soft sediment macrobenthic survey. Sediment samples from 13 stations (Fig. 1) were collected across an inshore to offshore transect from Jazan to the Farasan Islands using a 0.1 m2 Van Veen grab (two replicates at each site) and sieved through a 1 mm mesh screen. A total of 14 soft sediment stations were sampled. Sites located in the inner shelf include JAZ2, JAZ3, JAZ4, JAZ6, JAZ7, JAZ8, FI1, FI2, FI3, FI4, FI5 while sites located in the outer shelf included FI6, FI7, FI8. Samples were preserved in 96% ethanol. Sediment sub-samples from each replicate were taken for grain-size analysis, organic matter content (loss on ignition) and metals. Conductivity Temperature Depth (CTD) vertical casts were carried out at each station. The CTD casts recorded conductivity, temperature, depth and oxygen of the water column. Water samples were also taken for nutrients and chlorophyll a from the surface and the bottom layers (see below). In the laboratory, each sample was hand-sorted and then organisms identified using a stereomicroscope. Macrofauna were generally identified to the species level where possible or family level (see Supplementary Material). Sediment grain size was determined by wet sieving and calculation of dry weight percentage fractions following the Wentworth scale27. Grain size fractions were gravel (>2 mm), very coarse sand (1 mm), coarse sand (500 μm), medium sand (250 μm), fine sand (125 μm), very fine sand (63 μm) and silt-clay (8–10 m inner shelf (Table 3). Changes in size frequency and skewness. The corals surveyed ranged in diameter from 3 to 175 cm (Table 4). Statistically significant differences were detected between the size of the colonies from nearshore and offshore reefs for Acropora, Echinopora and Porites (Table 4). Smaller colonies were recorded in the nearshore reefs (Table 4). Juvenile coral density (mean ± SD) differed significantly between types of reefs for Acropora and Echinopora (p
